Abstract

In multispecies microbial communities, the exchange of signals such as acyl-homoserine lactones (AHL) enables communication within and between species of Gram-negative bacteria. This process, commonly known as quorum sensing, aids in the regulation of genes crucial for the survival of species within heterogeneous populations of microbes. Although signal exchange was studied extensively in well-mixed environments, less is known about the consequences of crosstalk in spatially distributed mixtures of species. Here, signaling dynamics were measured in a spatially distributed system containing multiple strains utilizing homologous signaling systems. Crosstalk between strains containing the lux, las and rhl AHL-receptor circuits was quantified. In a distributed population of microbes, the impact of community composition on spatio-temporal dynamics was characterized and compared to simulation results using a modified reaction-diffusion model. After introducing a single term to account for crosstalk between each pair of signals, the model was able to reproduce the activation patterns observed in experiments. We quantified the robustness of signal propagation in the presence of interacting signals, finding that signaling dynamics are largely robust to interference. The ability of several wild isolates to participate in AHL-mediated signaling was investigated, revealing distinct signatures of crosstalk for each species. Our results present a route to characterize crosstalk between species and predict systems-level signaling dynamics in multispecies communities.

Highlights

  • Microbes communicate with each other in order to coordinate behavior and gene expression through a process known as quorum sensing

  • Multiple species communicate using chemical signals, and crosstalk often governs the activities of microbial populations, including interactions with the host system, forming biofilms, and bioluminescence. Understanding such bacterial interactions is essential to control and prevent these population-level behaviors regulated by signal exchange

  • Quantifying bacterial crosstalk will help improve the robustness of synthetic cellular networks that utilize signal exchange

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Summary

Introduction

Microbes communicate with each other in order to coordinate behavior and gene expression through a process known as quorum sensing. Several Gram-negative bacteria use acyl-homoserine lactones (AHLs) as a signal to communicate [1,2,3,4,5,6]. These signaling systems typically consist of a synthase, such as luxI, which produces a variant of AHL, and a receptor, such as luxR, which binds to AHLs. The receptor enacts global changes in gene expression in response to high concentrations of AHLs. Over 150 quorum sensing systems have been characterized [7,8], with most species containing one or a few signaling pathways. Variation in the chemical structure of AHLs impacts both affinity for the receptor and the regulatory response [6,7,8]

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